Functional Organization of Squirrel Monkey Primary Auditory Cortex: Responses to Frequency-Modulation Sweeps

2005 ◽  
Vol 94 (2) ◽  
pp. 1299-1311 ◽  
Author(s):  
Benoit Godey ◽  
Craig A. Atencio ◽  
Ben H. Bonham ◽  
Christoph E. Schreiner ◽  
Steven W. Cheung

The squirrel monkey twitter call is an exemplar of a broad class of species-specific vocalizations that contain naturally voiced frequency-modulated (FM) sweeps. To investigate how this prominent communication call element is represented in primary auditory cortex (AI), neuronal receptive field properties to pure-tone and synthetic, logarithmically spaced FM-sweep stimuli in 3 barbiturate-anesthetized squirrel monkeys are studied. Responses to pure tones are assessed by using standard measures of frequency response areas, whereas responses to FM sweeps are classified according to direction selectivity, best speed, and speed tuning preferences. Most neuronal clusters respond to FM sweeps in both directions and over a range of FM speeds. Center frequencies calculated from the average of high and low trigger frequency edges of FM response profiles are highly correlated with pure-tone characteristic frequencies (CFs). However, bandwidth estimates are only weakly correlated with their pure-tone counterparts. CF and direction selectivity are negatively correlated. Best speed maps reveal idiosyncratically positioned spatial aggregation of similar values. In contrast, direction selectivity maps show unambiguous spatial organization. Neuronal clusters selective for upward-directed FM sweeps are located in ventral–caudal AI, where CFs range from 0.5 to 1 kHz. Combinations of pure-tone and FM response parameters form 2 significant factors to account for response variations. These results are interpreted in the context of earlier FM investigations and neuronal encoding of dynamic sounds.

2001 ◽  
Vol 85 (4) ◽  
pp. 1732-1749 ◽  
Author(s):  
Steven W. Cheung ◽  
Purvis H. Bedenbaugh ◽  
Srikantan S. Nagarajan ◽  
Christoph E. Schreiner

The spatial organization of response parameters in squirrel monkey primary auditory cortex (AI) accessible on the temporal gyrus was determined with the excitatory receptive field to pure tone stimuli. Dense, microelectrode mapping of the temporal gyrus in four animals revealed that characteristic frequency (CF) had a smooth, monotonic gradient that systematically changed from lower values (0.5 kHz) in the caudoventral quadrant to higher values (5–6 kHz) in the rostrodorsal quadrant. The extent of AI on the temporal gyrus was ∼4 mm in the rostrocaudal axis and 2–3 mm in the dorsoventral axis. The entire length of isofrequency contours below 6 kHz was accessible for study. Several independent, spatially organized functional response parameters were demonstrated for the squirrel monkey AI. Latency, the asymptotic minimum arrival time for spikes with increasing sound pressure levels at CF, was topographically organized as a monotonic gradient across AI nearly orthogonal to the CF gradient. Rostral AI had longer latencies (range = 4 ms). Threshold and bandwidth co-varied with the CF. Factoring out the contribution of the CF on threshold variance, residual threshold showed a monotonic gradient across AI that had higher values (range = 10 dB) caudally. The orientation of the threshold gradient was significantly different from the CF gradient. CF-corrected bandwidth, residual Q10, was spatially organized in local patches of coherent values whose loci were specific for each monkey. These data support the existence of multiple, overlying receptive field gradients within AI and form the basis to develop a conceptual framework to understand simple and complex sound coding in mammals.


2007 ◽  
Vol 98 (4) ◽  
pp. 2182-2195 ◽  
Author(s):  
Craig A. Atencio ◽  
David T. Blake ◽  
Fabrizio Strata ◽  
Steven W. Cheung ◽  
Michael M. Merzenich ◽  
...  

Many communication sounds, such as New World monkey twitter calls, contain frequency-modulated (FM) sweeps. To determine how this prominent vocalization element is represented in the auditory cortex we examined neural responses to logarithmic FM sweep stimuli in the primary auditory cortex (AI) of two awake owl monkeys. Using an implanted array of microelectrodes we quantitatively characterized neuronal responses to FM sweeps and to random tone-pip stimuli. Tone-pip responses were used to construct spectrotemporal receptive fields (STRFs). Classification of FM sweep responses revealed few neurons with high direction and speed selectivity. Most neurons responded to sweeps in both directions and over a broad range of sweep speeds. Characteristic frequency estimates from FM responses were highly correlated with estimates from STRFs, although spectral receptive field bandwidth was consistently underestimated by FM stimuli. Predictions of FM direction selectivity and best speed from STRFs were significantly correlated with observed FM responses, although some systematic discrepancies existed. Last, the population distributions of FM responses in the awake owl monkey were similar to, although of longer temporal duration than, those in the anesthetized squirrel monkeys.


2011 ◽  
Vol 106 (6) ◽  
pp. 2825-2837 ◽  
Author(s):  
Michael Trujillo ◽  
Kevin Measor ◽  
Maria Magdalena Carrasco ◽  
Khaleel A. Razak

Frequency-modulated (FM) sweeps are common components of vocalizations, including human speech. Both sweep direction and rate influence discrimination of vocalizations. Across species, relatively less is known about FM rate selectivity compared with direction selectivity. In this study, FM rate selectivity was studied in the auditory cortex of anesthetized 1- to 3-mo-old C57bl/6 mice. Neurons were classified as fast pass, band pass, slow pass, or all pass depending on their selectivity for rates between 0.08 and 20 kHz/ms. Multiunit recordings were used to map FM rate selectivity at depths between 250 and 450 μm across both primary auditory cortex (A1) and the anterior auditory field (AAF). In terms of functional organization of rate selectivity, three patterns were found. First, in both A1 and AAF, neurons clustered according to rate selectivity. Second, most (∼60%) AAF neurons were either fast-pass or band-pass selective. Most A1 neurons (∼72%) were slow-pass selective. This distribution supports the hypothesis that AAF is specialized for faster temporal processing than A1. Single-unit recordings ( n = 223) from A1 and AAF show that the mouse auditory cortex is best poised to detect and discriminate a narrow range of sweep rates between 0.5 and 3 kHz/ms. Third, based on recordings obtained at different depths, neurons in the infragranular layers were less rate selective than neurons in the granular layers, suggesting FM processing undergoes changes within the cortical column. On average, there was very little direction selectivity in the mouse auditory cortex. There was also no correlation between characteristic frequency and direction selectivity. The narrow range of rate selectivity in the mouse cortex indicates that FM rate processing is a useful physiological marker for studying contributions of genetic and environmental factors in auditory system development, aging, and disease.


1993 ◽  
Vol 70 (5) ◽  
pp. 1988-2009 ◽  
Author(s):  
S. P. Dear ◽  
J. Fritz ◽  
T. Haresign ◽  
M. Ferragamo ◽  
J. A. Simmons

1. In Eptesicus the auditory cortex, as defined by electrical activity recorded from microelectrodes in response to tone bursts, FM sweeps, and combinations of FM sweeps, encompasses an average cortical surface area of 5.7 mm2. This area is large with respect to the total cortical surface area and reflects the importance of auditory processing to this species of bat. 2. The predominant pattern of organization in response to tone bursts observed in each cortex is tonotopic, with three discernible divisions revealed by our data. However, although cortical best-frequency (BF) maps from most of the individual bats are similar, no two maps are identical. The largest division contains an average of 84% of the auditory cortical surface area, with BF tonotopically mapped from high to low along the anteroposterior axis and is part of the primary auditory cortex. The medium division encompasses an average of 13% of the auditory cortical surface area, with highly variable BF organization across bats. The third region is the smallest, with an average of only 3% of auditory cortical surface area and is located at the anterolateral edge of the cortex. This region is marked by a reversal of the tonotopic axis and a restriction in the range of BFs as compared with the larger, tonotopically organized division. 3. A population of cortical neurons was found (n = 39) in which each neuron exhibited two BF threshold minima (BF1 and BF2) in response to tone bursts. These neurons thus have multipeaked frequency threshold tuning curves. In Eptesicus the majority of multipeaked frequency-tuned neurons (n = 27) have threshold minima at frequencies that correspond to a harmonic ratio of three-to-one. In contrast, the majority of multipeaked neurons in cats have threshold minima at frequencies in a ratio of three-to-two. A three-to-one harmonic ratio corresponds to the "spectral notches" produced by interference between overlapping echoes from multiple reflective surfaces in complex sonar targets. Behavioral experiments have demonstrated the ability of Eptesicus to use spectral interference notches for perceiving target shape, and this subpopulation of multipeaked frequency-tuned neurons may be involved in coding of spectral notches. 4. The auditory cortex contains delay-tuned neurons that encode target range (n = 99). Most delay-tuned neurons respond poorly to tones or individual FM sweeps and require combinations of FM sweeps. They are combination sensitive and delay tuned.(ABSTRACT TRUNCATED AT 400 WORDS)


2013 ◽  
Vol 110 (5) ◽  
pp. 1087-1096 ◽  
Author(s):  
Heesoo Kim ◽  
Shaowen Bao

Cortical sensory representation is highly adaptive to the environment, and prevalent or behaviorally important stimuli are often overrepresented. One class of such stimuli is species-specific vocalizations. Rats vocalize in the ultrasonic range >30 kHz, but cortical representation of this frequency range has not been systematically examined. We recorded in vivo cortical electrophysiological responses to ultrasonic pure-tone pips, natural ultrasonic vocalizations, and pitch-shifted vocalizations to assess how rats represent this ethologically relevant frequency range. We find that nearly 40% of the primary auditory cortex (AI) represents an octave-wide band of ultrasonic vocalization frequencies (UVFs; 32–64 kHz) compared with <20% for other octave bands <32 kHz. These UVF neurons respond preferentially and reliably to ultrasonic vocalizations. The UVF overrepresentation matures in the cortex before it develops in the central nucleus of inferior colliculus, suggesting a cortical origin and corticofugal influences. Furthermore, the development of cortical UVF overrepresentation depends on early acoustic experience. These results indicate that natural sensory experience causes large-scale cortical map reorganization and improves representations of species-specific vocalizations.


2020 ◽  
Author(s):  
Jean-Pierre R. Falet ◽  
Jonathan Côté ◽  
Veronica Tarka ◽  
Zaida-Escila Martinez-Moreno ◽  
Patrice Voss ◽  
...  

AbstractWe present a novel method to map the functional organization of the human auditory cortex noninvasively using magnetoencephalography (MEG). More specifically, this method estimates via reverse correlation the spectrotemporal receptive fields (STRF) in response to a dense pure tone stimulus, from which important spectrotemporal characteristics of neuronal processing can be extracted and mapped back onto the cortex surface. We show that several neuronal populations can be found examining the spectrotemporal characteristics of their STRFs, and demonstrate how these can be used to generate tonotopic gradient maps. In doing so, we show that the spatial resolution of MEG is sufficient to reliably extract important information about the spatial organization of the auditory cortex, while enabling the analysis of complex temporal dynamics of auditory processing such as best temporal modulation rate and response latency given its excellent temporal resolution. Furthermore, because spectrotemporally dense auditory stimuli can be used with MEG, the time required to acquire the necessary data to generate tonotopic maps is significantly less for MEG than for other neuroimaging tools that acquire BOLD-like signals.


Nature ◽  
2003 ◽  
Vol 424 (6945) ◽  
pp. 201-205 ◽  
Author(s):  
Li I. Zhang ◽  
Andrew Y. Y. Tan ◽  
Christoph E. Schreiner ◽  
Michael M. Merzenich

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